Cultivated and Wild Olives in Crete, Greece—Genetic Diversity and Relationships with Major Turkish Cultivars Revealed by SSR Markers

Abstract

The genetic relationships between and within some traditionally grown cultivars of olive tree (Olea europaea L.) in Greece (island of Crete) and in Turkey were investigated. Cultivars from Crete included ‘Koroneiki’, ‘Throubolia’ and ‘Mastoidis’, while those from Turkey included ‘Samanli’ and ‘Gemlik’. Cultivars were represented by multiple genotypes of aged trees collected from the field, each one complying with established descriptors. Representative genotypes of wild olive trees from Crete were also employed. A total of 112 genotypes were analysed, employing seven microsatellite (SSR) loci yielding a total of 81 alleles, and reaching a cumulative probability of identity of 6.73 × 10−09 with a mean observed heterozygosity of 0.852. Analysis of molecular variance significantly partitioned genetic diversity between and within cultivars, albeit with no appreciable difference between the two levels of diversity. All cultivar genotypes aggregated along single, cultivar-specific clusters, pointing to human-driven selection. The two Turkish cultivars ‘Samanli’ and ‘Gemlik’ were grouped together. The Cretan cultivar ‘Throubolia’ grouped together with the two Turkish cultivars, indicating germplasm movement across the Aegean Sea during historical times. Some gene flow was observed between the Cretan cultivars and the native wild populations (likely feral forms). SSR alleles were ranked for their efficiency in discriminating the examined materials, thus establishing a molecular key for cultivar identification. An identification process is proposed including a classification binary tree and provided a method for sorting any new unknown material purportedly originating from any of the analysed cultivars.

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References

  1. Agiomyrgianaki A, Petrakis PV, Dais P (2010) Detection of refined olive oil adulteration with refined hazelnut oil by employing NMR spectroscopy and multivariate statistical analysis. Talanta 80:2165–2171. doi:10.1016/j.talanta.2009.11.024

    CAS  Article  PubMed  Google Scholar 

  2. Alba V, Montemurro C, Sabetta W, Pasqualone A, Blanco A (2009) SSR-based identification key of cultivars of Olea europaea L. diffused in Southern-Italy. Sci Hortic 123:11–16

    Article  Google Scholar 

  3. Baldoni L, Cultrera NG, Mariotti R, Ricciolini C, Arcioni S, Vendramin GG, Buonamici A, Porceddu A, Sarri V, Ojeda MA, Trujillo I, Rallo L, Belaj A, Perri E, Salimonti A, Muzzalupo I, Casagrande A, Lain O, Messina R, Testolin R (2009) A consensus list of microsatellite markers for olive genotyping. Mol Breed 24:213–231

    CAS  Article  Google Scholar 

  4. Bandelj D, Jakse J, Javornik B (2002) DNA fingerprinting of olive varieties by microsatellite markers. Food Technol Biotechnol 40:185–190

    CAS  Google Scholar 

  5. Belaj A, Satovic Z, Cipriani G, Baldoni L, Testolin R, Rallo L, Trujillo I (2003) Comparative study of the discriminating capacity of RAPD, AFLP and SSR markers and of their effectiveness in establishing genetic relationships in olive. Theor Appl Genet 107:736–744

    CAS  Article  PubMed  Google Scholar 

  6. Belaj A, Munoz-Diez C, Baldoni L, Satovic Z, Barranco D (2010) Genetic diversity and relationships of wild and cultivated olives at regional level in Spain. Sci Hortic 124:323–330

    CAS  Article  Google Scholar 

  7. Belaj A, Leon L, Satovic Z, De la Rosa R (2011) Variability of wild olives (Olea europaea subsp. europaea var. sylvestris) analyzed by agro-morphological traits and SSR markers. Sci Hortic 129:561–569

    Article  Google Scholar 

  8. Besnard G, Rubio de Casas R (2016) Single vs multiple independent olive domestications: the jury is (still) out. New Phytol 209:466–470

    Article  PubMed  Google Scholar 

  9. Besnard G, Khadari B, Navascues M, Fernandez-Mazuecos M, El Bakkali A, Arrigo N, Baali-Cherif D, Brunini-Bronzini de Caraffa V, Santoni S, Vargas P, Savolainen V (2013) The complex history of the olive tree: from Late Quaternary diversification of Mediterranean lineages to primary domestication in the northern Levant. Proc R Soc B 280(1756):20122833. doi:10.1098/rspb.2012.2833

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  10. Botstein D, White RL, Skolnick M, Davis RW (1980) Construction of a genetic-linkage map in man using restriction fragment length polymorphisms. Am J Hum Genet 32:314–331

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Bracci T, Sebastiani L, Busconi M, Fogher C, Belaj A, Trujillo I (2009) SSR markers reveal the uniqueness of olive cultivars from the Italian region of Liguria. Sci Hortic 122:209–221

    CAS  Article  Google Scholar 

  12. Breiman L, Friedman JH, Olshen RA, Stone CJ (1984) Classification and regression trees. Wadsworth International Group, Belmont ISBN-10: 0412048418

    Google Scholar 

  13. Breton C, Terral JF, Pinatel C, Medail F, Bonhomme F, Berville A (2009) The origins of the domestication of the olive tree. C R Biol 332:1059–1064

    Article  PubMed  Google Scholar 

  14. Cipriani G, Marrazzo MT, Marconi R, Cimato A, Testolin R (2002) Microsatellite markers isolated in olive (Olea europaea L.) are suitable for individual fingerprinting and reveal polymorphism within ancient cultivars. Theor Appl Genet 104:223–228

    CAS  Article  PubMed  Google Scholar 

  15. Colella C, Miacola C, Amenduni M, D’Amico M, Bubici G, Cirulli M (2008) Sources of verticillium wilt resistance in wild olive germplasm from the Mediterranean region. Plant Pathol 57:533–539

    Article  Google Scholar 

  16. Díaz A, de la Rosa R, Martin A, Rallo P (2006) Development, characterization and inheritance of new microsatellites in olive (Olea europaea L.) and evaluation of their usefulness in cultivar identification and genetic relationship studies. Tree Genet Genomes 2:165–175

    Article  Google Scholar 

  17. Diez CM, Trujillo I, Martinez-Urdiroz N, Barranco D, Rallo L, Marfil P, Gaut BS (2015) Olive domestication and diversification in the Mediterranean Basin. New Phytol 206:436–447

    CAS  Article  PubMed  Google Scholar 

  18. Dixon P (2003) VEGAN, a package of R functions for community ecology. J Veg Sci 14:927–930 R package version 2.0–3

    Article  Google Scholar 

  19. Erre P, Chessa I, Munoz-Diez C, Belaj A, Rallo L, Trujillo I (2010) Genetic diversity and relationships between wild and cultivated olives (Olea europaea L.) in Sardinia as assessed by SSR markers. Genet Resour Crop Evol 57:41–54

    Article  Google Scholar 

  20. Ganino T, Beghe D, Valenti S, Nisi R, Fabbri A (2007) RAPD and SSR markers for characterization and identification of ancient cultivars of Olea europaea L. in the Emilia region, Northern Italy. Genet Resour Crop Evol 54:1531–1540

    CAS  Article  Google Scholar 

  21. Hagidimitriou M, Katsiotis A, Menexes G, Pontikis C, Loukas M (2005) Genetic diversity of major Greek olive cultivars using molecular (AFLPs and RAPDs) markers and morphological traits. J Am Soc Hortic Sci 130:211–217

    CAS  Google Scholar 

  22. International Olive Council (2000) World catalogue of olive varieties. Madrid, Spain.http://www.internationaloliveoil.org/store/index/665-world-catalogue-of-olive-varieties-publications

  23. International Olive Council (2016) Market newsletter. No 108 – September 2016.http://www.internationaloliveoil.org/news/view/686-year-2016-news/762-market-newsletter-september-2016

  24. Ipek A, Barut E, Gulen H, Oz AT, Tangu NA, Ipek M (2009) SSR analysis demonstrates that olive production in the southern Marmara region in Turkey uses a single genotype. Genet Mol Res 8:1264–1272

    CAS  Article  PubMed  Google Scholar 

  25. Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106

    Article  PubMed  Google Scholar 

  26. Khadari B, Charafi J, Moukhli A, Ater M (2008) Substantial genetic diversity in cultivated Moroccan olive despite a single major cultivar: a paradoxical situation evidenced by the use of SSR loci. Tree Genet Genomes 4:213–221

    Article  Google Scholar 

  27. Lanza F (2011) Olive: a global history. Reaktion Books, London ISBN: 1861898681

    Google Scholar 

  28. Linos A, Nikoloudakis N, Katsiotis A, Hagidimitriou M (2014) Genetic structure of the Greek olive germplasm revealed by RAPD, ISSR and SSR markers. Sci Hortic 175:33–43

    CAS  Article  Google Scholar 

  29. Lopes MS, Mendonca D, Sefc KM, Gil FS, Machado AD (2004) Genetic evidence of intra-cultivar variability within Iberian olive cultivars. Hortscience 39:1562–1565

    CAS  Google Scholar 

  30. Lumaret R, Ouazzani N, Michaud H, Vivier G, Deguilloux MF, Di Giusto F (2004) Allozyme variation of oleaster populations (wild olive tree) (Olea europaea L.) in the Mediterranean basin. Heredity 92:343–351. doi:10.1038/sj.hdy.6800430

    CAS  Article  PubMed  Google Scholar 

  31. Lynch M (1990) The similarity index and DNA fingerprinting. Mol Biol Evol 7:478–484

    CAS  PubMed  Google Scholar 

  32. Mekuria GT, Collins G, Sedgley M (2002) Genetic diversity within an isolated olive (Olea europaea L.) population in relation to feral spread. Sci Hortic 94:91–105

    Article  Google Scholar 

  33. Mkize N, Hoelmer KA, Villet MH (2008) A survey of fruit-feeding insects and their parasitoids occurring on wild olives Olea europaeassp. cuspidate, in the Eastern Cape of South Africa. Biocontrol Sci Tech 18:991–1004

    Article  Google Scholar 

  34. Muzzalupo I, Stefanizzi F, Salimonti A, Falabella R, Perri E (2009) Microsatellite markers for identification of a group of Italian olive accessions. Sci Agric (Piracicaba, Braz) 66:685–690. doi:10.1590/S0103-90162009000500014

    CAS  Article  Google Scholar 

  35. Newton C, Lorre C, Sauvage C, Ivorra S, Terral JF (2014) On the origins and spread of Olea europaea L. (olive) domestication: evidence for shape variation of olive stones at Ugarit, Late Bronze Age, Syria—a window on the Mediterranean Basin and on the westward diffusion of olive varieties. Veg Hist Archaeobotany 23:567–575

    Article  Google Scholar 

  36. Nikoloudakis N, Banilas G, Metzidakis J, Gazis F, Hatzopoulos P (2003) Discrimination and genetic diversity among cultivated olives of Greece using RAPD markers. J Am Soc Hortic Sci 128:741–746

    CAS  Google Scholar 

  37. Noormohammadi Z, Hosseini-Mazinani M, Trujillo I, Ratio L, Belaj A, Sadeghizadeh M (2007) Identification and classification of main Iranian olive cultivars using Microsatellite markers. Hortscience 42:1545–1550

  38. Noormohammadi Z, Trujillo I, Belaj A, Ataei S, Hosseini-Mazinan M (2014) Genetic structure of Iranian olive cultivars and their relationship with Mediterranean's cultivars revealed by SSR markers. Sci Hortic 178:175–183

    CAS  Article  Google Scholar 

  39. Owen CA, Bita EC, Banilas G, Hajjar SE, Sellianakis V, Aksoy U, Hepaksoy S, Chamoun R, Talhook SN, Metzidakis I, Hatzopoulos P, Kalaitzis P (2005) AFLP reveals structural details of genetic diversity within cultivated olive germplasm from the Eastern Mediterranean. Theor Appl Genet 110:1169–1176

    CAS  Article  PubMed  Google Scholar 

  40. Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  41. Petrakis PV, Agiomyrgianaki A, Christophoridou S, Spyros A, Dais P (2008) Geographical characterization of Greek virgin olive oils (Koroneikicv.) using H-1 and P-31 NMR fingerprinting with canonical discriminant analysis and classification binary trees. J Agric Food Chem 56:3200–3207

    CAS  Article  PubMed  Google Scholar 

  42. R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna ISBN 3–900051–07-0, URL http://www.R-project.org/

    Google Scholar 

  43. Rohlf FJ (2008) NTSYSpc: numerical taxonomy system, ver. 2.21q. Exeter Publishing Ltd, Setauket

    Google Scholar 

  44. Roubos K, Moustakas M, Aravanopoulos FA (2010) Molecular identification of Greek olive (Olea europaea) cultivars based on microsatellite loci. Genet Mol Res 9:1865–1876

    CAS  Article  PubMed  Google Scholar 

  45. Sarri V, Baldoni L, Porceddu A, Cultrera NGM, Contento A, Frediani M, Belaj A, Trujillo I, Cionini PG (2006) Microsatellite markers are powerful tools for discriminating among olive cultivars and assigning them to geographically defined populations. Genome 49:1606–1615

    CAS  Article  PubMed  Google Scholar 

  46. Sefc KM, Steinkellner H, Wagner HW, Glössl J, Regner F (1997) Application of microsatellite markers to parentage studies in grapevine. Vitis 36:179–183

    Google Scholar 

  47. Sefc KM, Lopes S, Mendonca D, Dos Santos MR, Machado MLD, Machado AD (2000) Identification of microsatellite loci in olive (Olea europaea) and their characterization in Italian and Iberian olive trees. Mol Ecol 9:1171–1173

    CAS  Article  PubMed  Google Scholar 

  48. Sneath PHA, Sokal RR (1973) Numerical taxonomy: the principles and practice of numerical classification. W. H Freeman and Company, San Francisco

    Google Scholar 

  49. Terzopoulos PJ, Kolano B, Bebeli PJ, Kaltsikes PJ, Metzidakis I (2005) Identification of Olea europaea L. cultivars using inter-simple sequence repeat markers. Sci Hortic 105:45–51

    CAS  Article  Google Scholar 

  50. Therneau TM, Atkinson EJ (1997) An introduction to recursive partitioning using the RPART routine. Technical report 61, Mayo Foundation, Rochester, USA

  51. Trujillo I, Ojeda MA, Urdiroz NM, Potter D, Barranco D, Rallo L, Diez CM (2013) Identification of the worldwide olive germplasm bank of Cordoba (Spain) using SSR and morphological markers. Tree Genet Genomes 10:141–155

    Article  Google Scholar 

  52. Vossen P (2007) Olive oil: history, production, and characteristics of the world’s classic oils. Hortscience 42:1093–1100

    Google Scholar 

  53. Xanthopoulou A, Ganopoulos I, Koubouris G, Tsaftaris A, Sergendani C, Kalivas A, Madesis P (2014) Microsatellite high-resolution melting (SSR-HRM) analysis for genotyping and molecular characterization of an Olea europaea germplasm collection. Plant Genet Resour 12:273–277

    Article  Google Scholar 

  54. Yoruk B, Taskin V (2014) Genetic diversity and relationships of wild and cultivated olives in Turkey. Plant Syst Evol 300:1247–1258

    Article  Google Scholar 

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Acknowledgements

The research presented herein was funded by the Greek Secretariat for Research and Technology (GSRT), project Regional Innovation Pole of Crete, “i4Crete, A8—Integrated system of olive oil fingerprinting control and promotion—11RIPC06” to AGD and to ITM which was coordinated by the Heraklion Chamber of Commerce and Industry, Heraklion, Crete, Greece. Ms. M. Aksehirli-Pakyurek’s research visit to NAGREF was funded by an Erasmus fellowship administered by the Technological Educational Institute of Crete (Prof. Ioannis Vlahos). Thanks are due to Ms. Maria Pikraki and to Mr. Dimitriοs Giakoumakis for their assistance with SSR markers and to Ms. Irene Stratidaki (IMBB-FORTH) for assistance with the LICOR sequencer. Comments of the three anonymous reviewers are greatly appreciated.

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Correspondence to A. G. Doulis.

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Aksehirli-Pakyurek, M., Koubouris, G.C., Petrakis, P.V. et al. Cultivated and Wild Olives in Crete, Greece—Genetic Diversity and Relationships with Major Turkish Cultivars Revealed by SSR Markers. Plant Mol Biol Rep 35, 575–585 (2017). https://doi.org/10.1007/s11105-017-1046-y

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Keywords

  • Classification binary tree
  • Cluster
  • Cultivar
  • Germplasm movement
  • Wild olives